The interaction of human eosinophils and neutrophils with non-phagocytosable surfaces: a model for studying cell-mediated immunity in schistosomiasis

Glauert, Audrey M.; Oliver, Rhonda C.; Thorne, Kareen J. I.

doi:10.1017/s0031182000000986

Cited by 15 publications

(4 citation statements)

References 25 publications

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“…In contrast, killing of nonphagocytosable helminths such as S. mansoni schistosomula is initiated at extracellular sites of intimate contact between the PMN plasma membrane and parasite surface (39,40). PMN-mediated host defense against schistosome ova represents, however, an unusual and little-studied model of the effector function of leukocytes.…”

Section: Discussionmentioning

confidence: 99%

Role of granulocyte oxygen products in damage of Schistosoma mansoni eggs in vitro.

Kazura¹,

Brito

Rabbege

et al. 1985

J. Clin. Invest.

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The objectives of this study were to describe the ultrastructure of granulocyte-Schistosoma mansoni egg interaction and to determine the role of reduced oxygen products as effectors of cell-mediated damage to the parasite target. Granulocytes attached to the parasites and closely applied their plasma membranes to the microspicules of the egg shell 30 min after mixing in the presence of immune serum. By 4 h, the egg shell was fractured and granulocyte pseudopodia extended toward the underlying miracidium. Granulocyte attachment to eggs resulted in release of O-(030-0.52 nmol/min per 2 X 106 cells) and accumulation of H202 (0.14-0.15 nmol/min) in the presence of antibody or complement. Granulocytes reduced egg tricarboxylic-acid cycle activity and hatching by 283±0.9 and 35.2±2.8%, respectively (cell-egg ratio of 1,000: 1). Exogenous superoxide dismutase (10 M&g/ml) inhibited granulocyte toxicity for egg metabolic activity (3.0±2.1% reduction in acetate metabolism vs. 283±0.9% decrease in controls without superoxide dismutase, P < 0.0005) and hatching (12.5±1.8% reduction, P < 0.0005), whereas catalase and heparin had no effect. Inhibitors of myeloperoxidase (1 mM azide, cyanide, and methimazole) augmented granulocyte-mediated toxicity of egg tricarboxylic-acid cycle activity (44-58% reduction in activity vs. 31 and 35% reduction in controls), suggesting that H202 released from cells was degraded before reaching the target miracidium. Oxidants generated by acetaldehyde (2 mM)-xanthine oxidase (10 mU/ml) also decreased egg metabolic activity and hatching by 62.0±9.0 and 38.7±73%, respectively. Egg damage by the cell-free system was partially prevented by superoxide dismutase (26.5±4.2% reduction in egg tricarboxylic-acid cycle activity) and completely blocked by catalase (0% reduction in activity). These data suggest that granulocyte-mediated toxicity for S. mansoni eggs is dependent on release of 02 or related molecules. These oxygen products, unlike H202, may readily reach the target miracidium where they may be converted to H202 or other microbicidal effector molecules.

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Section: Discussionmentioning

confidence: 99%

Role of granulocyte oxygen products in damage of Schistosoma mansoni eggs in vitro.

Kazura¹,

Brito

Rabbege

et al. 1985

J. Clin. Invest.

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“…Areas, 10-20 #m in length, that contain no overlying grains alternate with areas that have the same overlying grain density as controls (Figs. [6][7][8][9]. The tegumental membrane which has no overlying grains is pentalaminar which is the normal structure of this membrane (see Fig.…”

Section: Lectin-mediated Adherence-electron Microscopymentioning

confidence: 99%

Human neutrophils endocytose multivalent ligands from the surface of schistosomula of Schistosoma mansoni before membrane fusion.

Caulfield¹,

Korman²,

Samuelson³

1982

The Journal of Cell Biology

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Human buffy coat cells adhering to schistosomula of Schistosoma mansoni that were preincubated in fluorochrome-conjugated concanavalin A (Con A), wheat germ agglutinin, lentil lectin, or purified IgG from a hyperimmunized rabbit, were examined by fluorescence and transmission electron microscopy and by freeze-fracture. All four fluorochromeconjugated multivalent ligands were homogeneously distributed on the parasite surface after preincubation. Within 1-3 h after the addition of cells, large areas of nonfluorescence, 10-20 #m in diameter, were seen on the parasite surface. In addition, the fluorochromes were observed in granules within the cells. Electron microscope autoradiography of worms preincubated with 1251-Con A showed silver grains evenly distributed over the tegumental membrane. After the addition of cells, grains were seen over phagolysosomes in the cytoplasm of neutrophils adhering to the parasites. In addition, no grains were present over large areas of the tegumental membrane, which still retained its normal architecture, or over fusions between the neutrophil plasma membrane and the outer tegumental membrane. Rabbit IgG formed an electron-dense layer on the tegumental membrane which was endocytosed by neutrophils. Both neutrophils and eosinophils fused with the parasite in areas containing no electron-dense material on the surface. It is concluded that human neutrophils will endocytose a variety of multivalent ligands from the surface of schistosomula, which probably accounts for the failure of neutrophils to kill the parasite and acts to clear the parasite surface of both antigen and antibody. Presumably, the components of the parasite surface which have originally bound the ligands are also endocytosed since surface components labeled by galactose oxidase and NaBaH4 are taken into cells when examined by light microscope autoradiography. Finally, membrane fusion occurs in areas devoid of multivalent glands, which suggests that these ligands serve to bring the cells and parasites close together; but the actual fusigens probably reside in the lipids in the outer tegumental membrane.Schistosomula, larvae of Schistosoma mansoni, can be destroyed in vitro by human eosinophils--but not by neutrophils--after the parasites are preincubated in heat-inactivated sera from patients with schistosomiasis (28). Eosinophil-mediated killing is caused by exocytosis of lysosomes onto the parasite surface (3,7,17), and subsequent damage to the tegumental membrane is caused by major basic protein (2) and possibly peroxidases to which the worm is quite sensitive (13). The neutrophils, on the other hand, do not exocytose their lysosomes but instead fuse their plasma membranes with the outer tegumental membranes of the schistosomula over areas as large as 8 #m in diameter (3).In these experiments, we have promoted adherence between human buffy coat cells and schistosomula with three lectins concanavalin A (Con A), wheat germ agglutinin (WGA), and lentil lectin (Len), as well as with IgG purified from a hyperimmu...

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“…In addition, immunoglobulin G (IgG) antibodies [368] and complement proteins [369], facilitate the attachment of the eosinophil to the parasite. Adhering eosinophils flatten and release granule proteins [370,371], and oxygen radicals [99,108,372], onto the surface of the parasite eventually leading to its destruction.…”

Section: Parasitic Infestationsmentioning

confidence: 99%

Pulmonary immune cells in health and disease: the eosinophil leucocyte (Part II)

Kroegel¹,

Warner²,

Jc³

et al. 1994

Eur Respir J

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The second part of this review on eosinophils focuses on biological cell functions and surveys the various deleterious mechanisms involved in the eosinophil-dominated inflammatory reaction. It discusses the possible pathogenic role of eosinophils in several eosinophil-related diseases, such as parasitic infections, interstitial lung disorders and bronchial diseases, graft rejection, vasculitic granulomatous disorders, pleural effusion, and bronchogenic tumours.The final section of the article highlights the possible recent pharmacological and future therapeutic approaches in modifying eosinophil recruitment and function. Eur Respir J., 1994, 7, 743-760 This paper is published as a follow-on to "Pulmonary immune cells in health and disease: the eosinophil leucocyte (Part I)"* (Eur Respir J, 1994; 7: 519-543). Biological cell functionsThe eosinophil mediates its effector functions through various distinct cellular mechanisms, namely nonoxidative, oxidative, and humoral mechanisms ( fig. 7). Nonoxidative mechanismsAs mentioned previously, the three basic proteins as well as eosinophil peroxidase (EPO) have toxic properties independent of molecular oxygen species. For instance, major basic protein (MBP) [323], eosinophil cationic protein (ECP) [324] and EPO in the presence of hydrogen superoxide and a halide [99] kill helminthic parasites in vitro. In addition, these proteins are toxic for tumour cells and/or mammalian cells [325], including human pulmonary parenchyma and interstitial matrix [326,327], cultured human lung epithelial cells [328], and guinea-pig respiratory epithelium [252, 253,329]. Furthermore, it has been demonstrated that MBP damages human bronchial epithelium, which consists of desquamation and destruction of ciliated cells [329]. Finally, release of their granule proteins by plateletactivating factor (PAF)-activated intact eosinophils has been shown to imitate the characteristic pathological findings of airway epithelium in asthma [330].In addition to their cytotoxic action, eosinophil cationic proteins at certain subtoxic concentrations also stimulate other inflammatory cells. For instance, MBP and ECP have been shown to degranulate platelets [305], induce histamine release from mast cells and basophils [240, 245,331], as well as superoxide anion generation and lysosomal enzyme release by human neutrophils [264].Finally, eosinophil proteins may affect airway muscle function and hyperresponsiveness. Recent reports investigating the effects of direct intratracheal instillation of purified eosinophil granule proteins on pulmonary function and airway responsiveness in primates [281,332] have shown that MBP induces a dose-related increase in airway responsiveness to inhaled methacholine. In the same model, both MBP and EPO caused a transient bronchoconstriction immediately after instillation, that resolved within 1 h. Interestingly, other eosinophil granular proteins failed to effect airway responsiveness or pulmonary function.Mode of action. The mode of action of these basic proteins is n...

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The interaction of human eosinophils and neutrophils with non-phagocytosable surfaces: a model for studying cell-mediated immunity in schistosomiasis

Cited by 15 publications

References 25 publications

Role of granulocyte oxygen products in damage of Schistosoma mansoni eggs in vitro.

Role of granulocyte oxygen products in damage of Schistosoma mansoni eggs in vitro.

Human neutrophils endocytose multivalent ligands from the surface of schistosomula of Schistosoma mansoni before membrane fusion.

Pulmonary immune cells in health and disease: the eosinophil leucocyte (Part II)

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